Predator-prey interactions are often viewed as evolutionary arms races; while predators improve their hunting behaviors and their ability to sneak up on their prey, the prey improve upon their abilities to detect and escape from their predators. The problem, of course, is that there is a trade-off between maintaining vigilance – the attention necessary to be consistently aware of others in the environment takes quite a bit of physical and mental energy – and doing all the other things that an animal must do, such as finding its own food. As a result of this trade-off, many social species, especially mammalian and avian species, have developed alarm calls. Alarm calls are specific vocalizations that signal the presence of a danger in the environment to nearby conspecifics, and sometimes contain additional information about the type of threat or predator.

As we’ve discussed before, subsequent to the introduction of predatory birds, howler monkeys on Barro Colorado Island near Panama rapidly developed an alarm call specific for those birds that indicated the presence of an avian predator; something like “danger from above!” That is, they did not merely adapt an already existing alarm call to the new predator, they developed an entirely new one.

In certain cases, prey species have developed the additional ability to eavesdrop on the alarm calls of other species, gaining access to an additional source of information relevant to the presence of danger in the environment. This ability could be the consequence of a learned association between the alarm calls of another species and the presence of the predator, or it could be due to certain auditory properties common to the alarm calls of both species, and innate. More research is required to tease apart these possibilities. However, until recently, it was thought that the ability to identify and react to the alarm calls of other species was only possible in species that already had vocal communication. Several years ago, however, researchers from Princeton University observed this behavior in an unlikely species – a non-vocal reptile – the Galapagos marine iguana (amblyrhynchus cristatus).

Figure 1: The Galapagos Marine Iguana.

Prior to this observation, it was thought that non-vocal species, who did not have alarm calls themselves, would not be able to associate complex auditory stimuli with the presence of a predator. The Galapagos iguana does not have any vocalizations; instead, they communicate by using visual and olfactory signals. However, they live among the Galapagos mockingbirds (buteo galapagoensis), a species that does have auditory vocalizations and specific alarm calls. Further, since iguanas primarily live on the rocky shoreline, they are often unable to view hawks (their main predator) until it is too late. If they had the ability to eavesdrop on the alarm calls of the mockingbirds, they would be able to engage their anti-predator behaviors significantly earlier and increase their chances of survival.

The researchers recorded two types of vocalizations from the Galapagos mockingbirds: their song calls and their alarm calls, and edited them into soundtracks each containing two or three examples of either type of call. The researchers would find a cluster of juvenile and female iguanas (the hawks mostly hunt for juvenile and female iguanas) in three different sites on the coast of Santa Fe Island, and would play back the various mockingbird calls through a portable speaker system.

Previous observational research indicated that upon detecting a hawk, iguanas who were aggregated in a cluster would scatter in different directions, perhaps in an attempt to confuse the predator. Upon playback, the researchers noted the behavior of the iguanas – and those behaviors were coded as “non-response,” “alert,” (head raise, orienting towards the sound), or “escape” (walking or running away).

Figure 2: The Galapagos Mockingbird.

Forty-five percent of iguanas showed vigilance behavior during the playback of the alarm call, compared with only 28.1% of iguanas during the playback of the mockingbird songs, which was a statistically significant difference. This suggests that the Galapagos iguanas are able to eavesdrop on the alarm calls of the mockingbirds and respond accordingly. However, in addition to type of playback, the time of day and data collection site were also significant factors in predicting the proportion of iguanas responding to the playbacks.

Figure 3: Proportion of iguanas responding, according to type of call and site.

At each site, the iguanas successfully differentiated between the alarm calls and the songs, responding with escape behaviors more often subsequent to the alarm call. This is the first experimental evidence that a non-vocal species associated the alarm call of a different species with the presence of a nearby predator.

What might account for the differential responses among recording sites? The authors speculate that differences in ambient noise could have contributed, resulting in changes in volume or sound quality. As each recording site was on the rocky coast of the island, the sound quality would be subject to wind and the sounds of the ocean. An alternative explanation, of course, is that there are true differences between the sites, perhaps owing to slight variations in predator behavior or mockingbird vocalizations. The fact that the hawks on Santa Fe island begin their hunts each day on the northern side of the island and proceed south throughout the day might indeed result in higher predation rates at site three. If the hawks are successful at site three on a given day, they might not have any reason to continue on to sites one or two.

Figure 4: Recording sites on the island, with the general hunting flight trajectory of the hawks indicated with an arrow.

It was also noted that the iguanas were more responsive to the playbacks earlier in the day. One possibility is that these cold-blooded reptiles are more responsive earlier in the day, when their body temperature is lower, and they therefore require more time to escape due to their reduced agility. As the day continues, the sun passes overhead, and their body heat increases, their ability to escape more quickly might improve. I’m not quite satisfied with this explanation, as I would expect the opposite, actually – for evasive responses to be higher when the iguanas have higher body temperature.

It is particularly impressive that these iguanas appear able to capitalize on the alarm calls of another species, the Galapagos mockingbird. And by considering the environmental constraints placed on these iguanas by their specific location on the coast of Santa Fe Island, the elegance of evolution and natural selection becomes apparent.

On Santa Fe Island, the hawks routinely approach on their hunting paths from the north. It might make sense, therefore, that the iguanas generally orient towards the north so that they would be able to see the hawks coming. However, marine iguanas such as these must orient their bodies directly towards the sun, or at 180 degree angles to it, in order to survive. Without this behavioral thermoregulation, they would quickly overheat and die. The realities of their environmental requirements are directly at odds: face north to anticipate predation, and risk overheating, or face the sun to avoid overheating, and risk being eaten by an unseen hawk. The ability to capitalize on the auditory alarm vocalizations of another species – especially a species less constrained by thermoregulatory requirements – could therefore provide significant benefit. The evolution of this ability would allow the iguanas to simultaneously maintain their body temperature while maintaining awareness of potential threats of predation.

In order to confirm this evolutionary explanation, more research would be required to identify whether naive Galapagos iguanas, never exposed to the threat of predation or the calls of the mockingbirds, would recognize and respond to the alarm calls. The other possibility is that this is simply the result of associative learning of complex auditory information. In either case, the eavesdropping ability of this non-vocal reptile species is remarkable. For these iguanas, it truly is a sin to kill a mockingbird.

Comments

Having some experience with green iguanas in captivity, I know that they do vocalize (hissing), and will respond to hisses, clicks, and other noises in their environment. I wasn’t aware that marine iguanas didn’t vocalize similarly. I have to wonder at what point in their evolution the vocalizations were lost, and whether that plays a factor — if it’s only been a relatively short time (evolutionarily speaking) since the ability to vocalize was lost, it would make sense that they might yet retain a more complex relationship with auditory signals.

It is definitely possible that it worked the other way around, but I think it’s significant that some of the most ancient orders of reptiles (crocodilians and chelonians) are known to vocalize, often in quite complex ways. If the older orders are verbal creatures, it seems to make sense that vocal capabilities were gradually lost through evolution, rather than the other way around. But then, evolution is often a convoluted process.

I’m intrigued by the differences in time of day and site, and wonder how theses scale/compare to other sites, islands, and seasons. Random thoughts:

Santa Fe is one of the smaller islands in the archipelago, and certainly not the only one with iggies, mockingbirds or hawks (and though I can’t say for certain without checking, I don’t think it’s the only spot where the three coincide). We know that populations of finches famously vary between islands (in diet, beak shape, and behaviour), so it’s quite possible that the observed relationship varies too.

Even on the one island, how does the east shore compare to the west? Is this phenomenon observed only in this area due to the proximity of a popular hawk nesting site?

And what about during mating season? The researchers tested playback on clusters of females and juveniles, reportedly the hawks’ coveted target. During mating season, though, male A. cristatus turn bright red. This makes them more visible on the rock face; I wonder if it makes them more attractive targets too. Does it alter the hawks’ feeding preferences? Does it change the listening dynamics among the iggies? Does it matter if there are many Sally Lightfoot crabs around (they’re bright red and often comingle with the iguanas)?

Actually, the temperature effect is in line with what’s already known about behavioral responses to threats in lizards at various temperatures. Spring speed in lizards is strongly influenced by temperature (because it’s all about the rate of reactions, notably muscle twitch kinetics and the force-velocity relationship). However, bite force is not, because muscle isometric force (force at a constant length) is not dependent upon temperature (once they’re attached to the actin, the myosin heads stay that way w/o any energy, which is why rigor mortis occurs). Thus, at cold temperatures, lizards are more likely to turn and fight, while at warm temperatures, they’re more likely to run. http://mama.indstate.edu/angillet/BIOL101/Labs/References/Bennett%201980.pdf

It is definitely possible that it worked the other way around, but I think it’s significant that some of the most ancient orders of reptiles (crocodilians and chelonians) are known to vocalize, often in quite complex ways. If the older orders are verbal creatures, it seems to make sense that vocal capabilities were gradually lost through evolution, rather than the other way around. But then, evolution is often a convoluted process.